~2-6989~8 $3.00 + 0.00 Copyright 0 1988 Pergamon Press plc
V&ion f&s. Vol. 28, No. 11, pp. 1235-1246, 1988 Printed in Great Britain. All rights reset&
AGING,
SENILE MIOSIS AND SPATIAL CONTRAST SENSITIVITY AT LOW LUMINANCE
MICHAEL E. SLOANE’, CYNTHIA OWSLEY~ and SARAL. ALVAREZ) ‘Department of Psychology, *Department of Ophthalmology, School of Medicine/The Eye Foundation Hospital and %chool of Optometry, University of Alabama at Birmingham, Birmingham, AL 35294, U.S.A. (Received 30 October 198f; in revisedform 22 March 1988) purpose of this study was to determine how aging affects spatial contrast sensitivity at low light levels and to examine whether senile miosis, which reduces retinal illuminance in the aged eye, underlies any observed sensitivity loss. Contrast thresholds for targets having a range of spatial frequencies were measured in young (n = 13, M age = 24) and older (n = 11, M age = 73) adults who were free from identifiable ocular pathology. Measurements were carried out at three luminance levels spanning a three log unit range. Results indicated that older adults’ loss in contrast sensitivity not only increased with increasing spatial frequency, but also became more pronounced with decreases in luminance. level. Additional threshold measurements where pupil diameter was varied indicated that senile miosis was not responsible for older adults’ loss in spatial vision at any light level tested. Rather, older adults’ miotic pupil tended to have a positive effect on their spatial vision in that it slightly improved their contrast sensitivity. Abstract-The
INTRODUCTION
Studies on how aging affects spatial vision have indicated that older adults tend to exhibit losses in contrast sensitivity at higher spatial frequencies, even when they are considered dinically normal (e.g. Derefeldt et al., 1979; Owsley et al., 1983). Currently there is wide disagreement as to the role of neural vs optical factors underlying this deficit. Several studies have examined “neural” contrast sensitivity using laser interferometric techniques which purportedly bypass the optics of the eye, but the results of these studies have been mixed. Dressler and Rassow (198 1) and Kayazawa et al. (198 1) note that there is no change in neural contrast sensitivity throughout adulthood, whereas Morrison and McGrath (1985) in a detailed study find that neural contrast sensitivity declines dramatically with age. Other studies have argued that optical mechanisms underlie the age-associated deficit. For example, Hemenger (1984), on the basis of a mathematical analysis, argues that increased intraocular light scatter due to agerelated changes in the ocular media can fully account for older adults’ loss in high frequency sensitivity. Several investigators (Owsley et al., 1983; Wright and Drasdo, 1985; Sturr et al., 1986) have suggested that the reduced retinal illuminance of the aged eye, stemming from
senile miosis and increased lenticular density, can account for much of older adults’ sensitivity loss. Thus, it is obvious that there is little concensus about what mechanisms underlie older adults’ loss of spatial contrast sensitivity. In the present study we attempt to eliminate some of this confusion by specifically examining the ~ont~bution of senile miosis. Senile miosis refers to the tendency of the older adult’s pupil to remain at a small diameter despite decreases in ambient illumination (Kornzweig, 1954; Loewenfeld, 1979). Under normal circumstances the pupil of the young adult increases in diameter with decreases in light level. Woodhouse (1975) has demonstrated that the pupil (in younger adults) assumes a diameter which optimizes spatial resolution, by balancing the positive vs negative effects of retinal illuminance changes and optical aberration. For example, a large pupil will increase retinal illumination, thereby improving resolution (up to a point), but it will also lead to heightened optical aberration which will hamper resolution. Thus, this delicate balance is likely to be disrupted in the older eye where the pupil remains at a small, relatively fixed size. It is important to note that senile miosis is not a problem for older adults at high light levels (e.g. 100 cd/m*), since younger and older adults
1235
1236
MICHAEL E. SLOANE
typically have similar pupil diameters under these conditions, usually between 2 and 4mm. Furthermore, Woodhouse (1975) has shown that spatial resolution at this high luminance is unaffected by pupil size changes within this range. However, the situation is quite different at lower luminance levels. As luminance decreases, the younger adult’s pupil increases in size, thereby increasing retinal illuminance. However, the older adult’s pupil remains at a small size. For example, at 0.1 cd/m2, the young adult’s pupil is typically around 6 mm in diameter, whereas the older adult’s pupil is typically around 2-4 mm. Woodhouse (1975) has shown that spatial resolution in younger adults deteriorates significantly at this luminance level when pupil diameter is experimentally decreased from 6 to 2 mm. Therefore, one might expect that the older adult’s small pupil may lead to a significant loss in spatial vision at lower light levels. Despite the above observations on senile miosis, there has been relatively little research devoted to older adults’ visual abilities at lower iight levels under steady-state conditions, such as in a dimly-lit room, at twilight, or at night. In fact, virtually all of the studies on aging and contrast sensitivity referred to earlier have been limited to photopic light levels. This is rather surprising, not only because of the retinal illuminance reduction associated with senile miosis, but also because older adults themselves report that “seeing under conditions of poor illumination” is one of their major visual problems (Kosnik et al., 1988). Yet, despite these selfreports as well as clinical impressions, this area of study has been largely neglected. In a previous study on this topic, Richards (1977) measured letter acuity at a range of luminance levels in adults of various ages. Results indicated that while adults of all ages had acuity reductions with decreases in chart luminance, older adults suffered from far greater reductions than did younger adults. However, it is difficult to ascertain from this study the actual severity of older adults’ vision loss, or the mechanisms which underlie it, since subjects were not screened for cataractous lens changes and were not refracted for the test distance. The goal of the present research, then, is two-fold: (1) to determine how older adults’ loss in spatial contrast sensitivity changes as a function of luminance level; and (2) to examine to what extent senile miosis underlies any observed contrast sensitivity loss.
et al.
EXPERIME~
1
Before
directly addressing the issue of senile the first study was designed to examine how aging affects spatial vision as a function of steady-state adaptation level (see Barlow, 1972). Spatial contrast sensitivity was measured over a 3 log Unit range of luminance, spanning the photopic region to the border of the scotopic/mesopic region (Le Grand, 1972). For younger adults, it is well-established that spatial contrast sensitivity decreases with decreasing background ilIumination (Schade, 1956; Bryngdahl, 1965; Van Nes and Bouman, 1967; Kelly, 1972; De Valois et al., 1974). The contrast sensitivity function is not simply displaced downward as adaptation level decreases; instead, higher spatial frequencies suffer from relatively greater losses in sensitivity than do lower frequencies, thus shifting the peak of the function leftward to lower spatial frequencies. These psychophysical changes may reflect receptive field changes in retinal and LGN cells as luminance decreases, such as the inhibitory surround becoming less effective at low light levels (Barlow et al., 1975; Derrington and Lennie, 1982; Kaplan et al., 1979). miosis,
Method Subjects. Two groups of observers were tested: 13 young adults, mean age 24, age range 19-35; and I1 older adults, mean age 73 yr, age range 67-79. Written informed consent was obtained from each participant after the nature and purpose of the study were explained. Young adults were students or employees at the university and were in good ocular health as indicated by their most recent eye exam. Mean letter acuity for young adults was 0.84 min arc (SEM = 0.03). Acuity was tested on a standard high-contrast (0.90), high-luminance (72.1 cd/ m’) letter chart utilizing Sloan letters. Older adults were recruited from the Primary Care Clinic or from a senior citizens meeting center. All were living inde~ndently in the community and were in good general health. Detailed eye examinations were performed on all older participants, which included direct and indirect ophthalmoscopy, biomicroscopy, applanation tonometry, distance refraction, and visual field assessment using a tangent screen. Mean letter acuity for older adults was 1.16 min arc (SEM = 0.05). All older adults were judged to be in good ocular health and did not exhibit drusen, although they did exhibit ocular
Aging, senile miosis and spatial vision
changes typical of old age, such as increased lenticular density and subtle macular changes. The important point is that these individuals did not reveal any frank pathological signs and would be considered by most eye care specialists to be in good eye health. In selecting these older adults for our sample, we recognize that there is an arbitrary line between what one considers good eye health in the elderly vs the beginning stages of pathological or vision threatening processes (Johnson, 1985; Johnson and Choy, 1987). In addition, we are artificially restricting the heterogeneity of the older age group by limiting our sample to older adults who must meet strict ophthalmological criteria (Rowe and Kahn, 1987). Our goal in studying this population of older adults stems from our interest in older adults who are thought to have few visual problems based on traditional clinical information, yet often complain of serious visual difficulties which require documentation (Kosnik et al., 1988). Stimuli. Targets consisted of vertical sinusoidal gratings having a range of spatial frequencies (0.5, 1, 2, 4, 8, and 11.4c/d) and were counterphase flickered at a rate of 0.5 Hz. Gratings were generated by a CS-2000 Contrast Sensitivity System (Nicolet) and displayed on a television monitor. Targets were circular and subtended a visual angle of 6”. The rectangular surround screen was large, subtending 61 x 51” of visual angle, and was matched in luminance to that of the target in each luminance condition Maximum target contrast was 0.70, where contrast is defined as the difference between maximum and minimum luminances, divided by their sum. Targets were presented at 3 luminance levels: 107,3.38, and 0.107 cd/m2, spanning a 3 log unit range of luminance. Luminance was set at the appropriate level by positioning glass neutral density filters in front of the subject’s eye. An opaque black cloth was draped around the subject’s head to block out any stray light that might have entered the subject’s eye. Procedure. Contrast thresholds for targets of each spatial frequency in each luminance conditions were measured using a tracking procedure (Sekuler and Tynan, 1977). The procedure used in the present study was highly similar to that used in our earlier work (Owsley et af., 1983). Before the threshold measurement procedure began for a grating of a given spatial frequency, that grating was initially presented for 2 set at a suprathreshold contrast (0.50). The purpose
1237
of this “preview” was to minimize the effects of spatial frequency uncertainty (Davis and Graham, 1981). After 3 see blank screen, a high tone indicated that testing was beginning. The grating was initially presented at a ~ndomlydetermined, near-zero, subthreshold contrast; contrast was then gradually increased. The observer’s task was to press a button when the bars first came into view, which then signalled the computer to begin decreasing contrast. The observer was instructed to keep the button pressed as long as the bars were visible; when the bars were no longer visible, the subject was asked to release the button. The button’s release signalled the computer to increase contrast, and the cycle was begun again. The tracking procedure ended after eight contrast reversals. A preview of the next spatial frequency was then presented followed by threshold measurement for that target, Threshold for a given spatial frequency was defined as the geometric mean of the eight contrast reversals. Before beginning formal data collection, subjects were given practice at a low and a high spatial frequency to insure that they understood the task. A tracking method was chosen over other psychophysical measurement procedures since our earlier work showed it to be a rapid and efficient way to measure thresholds in older adults (Owsley et al., 1983). Reaction time differences between young and older adults do not pose a problem since in the tracking method, threshold is approached from both above and below, so reaction time effects per se are averaged out. In addition, studies using the tracking method have found aging-related changes in contrast sensitivity that are similar to those trends reported in studies using forcedchoice procedures, which are relatively free of criterion effects (Morrison and Reilly, 1986; Higgins et al., 1983). Subjects were adapted to the light level in a given condition for 5-10 min before testing was begun. Measurements were first done at the highest light level and then at the successively dimmer levels. This order was chosen so that during the course of the experiment, subjects would not have to adjust to radically different luminance levels on successive runs. Pilot testing indicated that subjects found it more comfortable to begin the experiment with the highest light level (the targets were “easier to see”), and also that the order of the luminance conditions had no effect on contrast sensitivity. Testing was monocular. The tested eye was
1238
MICHAEL E. SLOANE et al.
refracted for the target distance (both spherical and cylindrical components). Trial lenses were positioned in front of the subject’s eye if a correction was required. The untested eye was occluded with frosted glass which permitted light to pass, but made pattern invisible. Neutral density filters were also placed in front of the occluded eye, when appropriate, in order to match the luminan~ level of the untested eye to that of the tested eye. Pupil diameter in all subjects was measured under each luminance condition. The luminance levels used in the experiment were re-created in the hemisphere of a Goldman perimeter. The subject was asked to gaze into the perimeter at the fixation marker, and the experimenter then measured the diameter of the pupil using the perimeter’s telescope and millimeter reticule. Because the lowest Iuminance condition was so dim (0.107 cd/m’), the pupil could not be distinctly seen through the perimeter’s telescope. But the pupil was visible if the experimenter looked directly at the subject from the side of the perimeter; thus, to estimate pupil diameter at the lowest light level, the experimenter used a small ruler with millimeter steps.
with increasing spatial frequency. Second, older adults’ deficit in spatial vision becomes more pronounced with decreasing luminance. For illustrative purposes, the data for each luminance level were fit by second-order polynomials which accounted for a large proportion of the variance at each luminance level (r’= 0.95 at 107 cd/m2; r* = 0.94 at 3.38 cd/m’; T’ = I .OO at 0.107 cd/m’). Admittedly, there are only three points entered into the polynomial fit at the lowest luminance; however, this is because older adults’ sensitivity was so poor at higher frequencies, their thresholds could not be measured in our apparatus. Thus, even though the higher spatial frequency points cannot be placed on this graph, older groups’ vision loss is most likely as severe as the polynomial function
107 cd /m2 2.5
b
0.5
Results
Figure 1 displays the results of Expt 1. Panel a contains the results from lO?cd/m*, Panel b the results from 3.38 cd/m*, and Panel c the results from 0.107 cd/m2. Contrast sensitivity (reciprocal of contrast threshold) is plotted as a function of spatiai frequency on log-log coordinates, for each luminance level tested. Both age groups exhibited the characteristic decline in spatial contrast sensitivity, especially at higher frequencies, that accompanies decreases in target luminance. However, at all luminance levels tested, older adults had significant losses in sensitivity as compared to young adults, which was confirmed by statistical analysis (F-test): At 107 cd/m*, P < 0.~1 at all frequencies; at 3.38 cd/m’, P < 0.001 at all frequencies; at 0.107 cd/m’, P < 0.0001 at all frequencies. Table 1 lists mean contrast threshold and standard error of the mean (SEM) in each luminance condition for both age groups. To better illustrate older adults’ loss in spatial contrast sensitivity, Fig. 2 shows the difference in mean log sensitivity for young and older adults as a function of spatial frequency, with a separate function for each luminance level. There are two notable features of Fig. 2. First, older adults’ loss in contrast sensitivity increases
fa)
c
t I
1 3.38 cd/m2 f‘F -is c t e E 8
old
I
(b)
2.5 2.0 1.5 YounO
1 .o
I-
0.107 cd/m*
2.5
Spatial
(c)
frequency (c/deg)
Fig. I. Mean contrast sensitivity as a function of spatial frequency on log-log coordinates, for young and older groups.Panel a, data from 107 cd/m? Panel b, 3.38 cd/m? Panel c, 0.107 cd/m*. Solid lines represent data for young adults; dashed lines, older adults. See Table 1 for variability.
1239
Aging, senile miosis and spatial vision Table 1. Mean contrast threshold and SEM in Expt 1 107 cd/m* Old Young 0.5 c/d Mean SEM 1 c/d Mean SEM 2 c/d Mean SEM 4 c/d Mean SEM 8 c/d Mean SEM 11.4 c/d Mean SEM
3.38 cd/m2 Young Old
0.107 cd/m* Old Young
-1.799 0.033
-1.638 0.040
-1.939 0.023
-1.723 0.042
-1.397 0.039
-1.037 0.067
-2.189 0.036
-1.991 0.056
-2.193 0.034
-1.977 0.048
-1.528 0.040
-1.127 0.071
-2.379 0.030
-2.t99 0.045
-2.229 0.042
-1.882 0.055
-1.401 0.054
-0.857 0.101
-2.365 0.043
-2.083 0.055
-1.938 0.053
-1.485 0.057
-1.048 0.065
-*
-1.948 0.078
-1.591 0.073
-1.441 0.080
-0.970 0.085
-0.474 0.067
-*
-1.600 0.075
- 1.230 0.061
-0.986 0.084
-0.358 0.093
-*
_*
*Over 50% of the subjects in the group could not detect the target at maximum contrast (70%). so these data points have been omitted from statistical consideration.
suggests since even at 70% contrast, they still could not see the target, Figure 3 displays mean pupil diameter for young and older subjects in each luminance condition. Our data are in good agreement with the earlier work on senile miosis referred to previously. At the highest lminance tested, 107 cd/m’, pupil diameter is very similar in the two age groups. As luminance decreases, the young adult’s pupil characteristically increases in size from about 4 to 6 mm, whereas for the older adult, increases in pupil size are very minima1 or nonexistent. By measuring pupil size in the perimeter, we probably have slightly underestimated pupil size in our young adults during contrast sensitivity testing. Since pupillary constriction is associated with increased
a~ommodation (Knoll, 1949), one would expect pupil diameter in our young adults to be smaller in the perimeter (viewing distance 30cm) than during the threshold measurement task (viewing distance 200 cm). This expectation was later confirmed by measurements on three young subjects (age range 31-34 yr); decreasing their accommodative demand by 3 D increased their pupil diameter by OS-l.0 mm on average. In terms of the present study, this simply means that the pupil differences in our young vs older adults are even greater than the differences illustrated in Fig. 3. Discussion
The results of Expt 1 confirm a common subjective complaint of older adults that they experience significant visibility problems under conditions of reduced luminance. Our data not only indicate that older adults’ loss in spatial vision becomes more serious with increasing 8 -7
107 cd/m’
3.38
cd/m2
0.107cd/mz
E6 10
1
Spatial
frequency
100
(c/deg)
Fig. 2. Difference in mean log contrast sensitivity between young and old groups, as a function of spatial frequency, at three luminance levels. Open circles, 107 cd/m*; open triangles, 3.38 cd/m*; open squares, 0.107 cd/m*. Solid lines are second-order polynomial functions fit to data; see text for further details.
f 5 6 E4 .$ 3 .k P = 2 a 1 Yng
Old
Yng
Old
Yng
Old
Fig. 3. Mean pupil diameter (mm)for young and old groups at each luminance level tested (as labelled).
I240
MICHAEL E. %OANE
frequency, agreeing with earlier work (Owsley et al., 1983), but also point out that this vision loss becomes exacerbated under low environmental light levels. Unlike our earlier work (Owsley et al., 1983), mean contrast sensitivity at the lowest spatial frequency for older adults was slightly worse (about 0.2 log units) than that of young adults. This small, but statistically reliable difference may arise from differences in the targets used in the two studies. Gratings in this experiment were counterphase flickered at a rate of 0.5 Hz, whereas in the earlier study gratings were stationary. Since older adults tend to have elevated thresholds for temporally-modulated targets (Sekuler et al., 1980; Owsley et al., 1983), this may be why a sensitivity loss was observed in the present study. Another possible explanation for this sensitivity difference may be due to the fact that in this study the target was relatively large (circular 6”), 2” wider than that used in the earlier study, thus permitting more cycles of the target to be displayed. Previous work has indicated that sensitivity to low spatial frequencies tends to improve with increases in the number of cycles/display (Kelly, 1977; McCann et af., 1978). While this may be the case for younger adults, it could be that older adults do not benefit similarly from increases in display size. This possibility is consistent with the finding that older adults tend to have decreased spatial summation when compared to younger adults (Owsley and Sekuler, 1982). Further work could resolve this issue by examining how display size differentially affects thresholds in young vs older adults. Relevant to our finding that older adults experience visibility problems at low light levels under steady-state conditions, is the extensive literature on a related visual function, dark adaptation (summarized in Pitts, 1982; Weale, 1982). These studies suggest that older adults have elevated thresholds throughout the entire time-course of adaptation to darkness, although the rate of sensitivity recovery apparently does not change (Birren and Shock, 1950; Eisner et al., 1987). The specific magnitude of the age effect varies across studies, most likely due to variables such as stimulus characteristics (e.g. wavelength of test target) and the eye health of older subjects. In addition, there seems to be little agreement about what mechanisms underlie older adults’ difficulties in dark adaptation. Some researchers have suggested that lenticular changes and senile miosis can largely account
et al.
for the threshold elevation (Robertson and Yudkin, 1944; Weale, 1982), while others have argued that neural and metabolic factors also play a significant role (McFarland et al., 1960; Pitts, 1982). Therefore, further work could fruitfully examine these arguments, and also relate data collected under steady-state adaptation (as in the present study) to data collected during temporal adaptation (see Barlow, 1972). Given that Expt 1 has demonstrated that older adults have significant losses in spatial contrast sensitivity which are exacerbated under low light levels, the question becomes, what mechanisms underlie this vision loss? As discussed earlier, one of the most obvious issues to address is the role of senile miosis, since it reduces retinal illuminance in the older eye and thus could theoretically hamper spatial vision. EXPERIMENT
2
It has been widely noted that retinal illuminance is substantially reduced in the older eye (Weale, 1963; van Norren and Vos, 1974; Blackwell and Blackwell, 1979); most of this light reduction has been attributed to senile miosis, with the balance thought to be due to increased lenticular absorption and light scatter in the older eye. For example, Weale (1961) has noted that the 60-yr-old retina receives about onethird the light as the 20-yr-old retina. The psychophysical data are consistent with this estimate; older adults’ contrast thresholds for spatial targets can be made similar to those of young adults by raising light levels by a factor of 2-3 (Guth, 1957; Blackwell and Blackwell, 1979; Owsley et al., 1983). This relationship between retinal illuminance differences between the young and old eye, on the one hand, and the threshold data on the other, has led researchers to conclude that senile miosis is largely responsible for older adults’ threshold elevations (Pitts, 1982; Owsley et al., 1983; Wright and Drasdo, 1985). However, it is important to point out that this relationship between retinal illuminance differences and psychophysical differences is correlational, and thus does not permit inferences about cause and effect. While senile miosis could be the basis for older adults’ sensitivity loss, the research to date has never specifically addressed this issue. Furthermore, in suggesting that senile miosis underlies older adults’ sensitivity losses, one is assuming that a small pupil diameter only has negative effects (i.e. reducing
Aging, stile miosis and SPati&Vision
retina1 illuminance). But, in fact, a small pupil can also be beneficial for vision in that it minimizes optical aberration and increases depth-of-focus. This increased depth-of-focus is greatest at lower spatial frequencies which are particularly impo~nt for individuals with reduced acuity and for vision at low luminance (Legge et al., 1987). Senile miosis could conceivably be an “adaptive” mechanism counteracting the negative effects of various agingrelated changes in the eye and visual system. It appears that previous research may have been premature in suggesting senile miosis as a major factor underlying older adults’ threshold problems. Given these considerations, then, the present experiment examined the effect of pupil size on spatial contrast sensitivity in young and oIder observers. Unlike Campbetl and Green (1965), we examined the effects of pupil diameter without compensating for changes in retinal illumination. Measurements were made at several luminance levels, in order to evaluate the h~othesis that senile miosis underlies older adults’ accentuated losses at low light levels. Method Subjects. The experiment involved a subset of the subjects tested in Expt 1, who were selected on the basis of their availability to return to the laboratory for further testing. There were 8 young subjects (mean age 24, range 19-35) with mean acuity 0.78 min arc, and 7 older subjects (mean age 74, range 67-79) with mean acuity 1.17min arc. Stirnu~~and procedure. Stimuli were generated and displayed in the same fashion as Expt 1, and were presented at the same three light levels. Contrast thresholds for each subject were measured at several different pupil diameters. The threshold measurement task was identical to that used in Expt 1. The following procedure was used to achieve a range of pupil sizes in each subject. A drop of 0.5% tropicamide (Mydriacil, Alcon Inc.) was administered to the eye to be tested in order to dilate the pupil. After the pupil had time to dilate to its maximum size for that drug dosage (around 20-30min), pupil diameter was measured using the same technique as in Expt 1. Contrast thresholds were then measured for gratings of each spatial frequency, at each of three luminance levels. Following testing, pupil diameter was measured again. The subject was then asked to sit in the waiting room during which time the dilation began to wear off. After about 30-45 min. the
1241
pupil was then remeasured, and if the pupil diameter had decreased, contrast sensitivity testing was carried out again. The pupil diameter was then remeasured, and the subject once again rested in the waiting room. This cycle was repeated until the pupil returned to its habitual diameter under 107 cd/m’. In this fashion, spatial contrast sensitivity for the three luminance levels was measured for 2-4 pupil diameters in each subject. The number of actual pupil sizes measured in each subject varied across subjects because of individual differences in the maximum pupil diameter achieved after administration of the tropicamide and in how rapidly the drug wore off. The entire laboratory visit lasted from 5-6 hr, but only about 2 hr were spent in actual psychophysical testing. In pilot work we were interested in whether there may be significant changes in refractive error in either age group after dilation, which would complicate interpretation of the contrast sensitivity data in the dilated conditions. Refractive error (spherical and cylind~cal components) and letter-acuity were measured before and after dilation in 8 young (mean age 26, range 19-35) and 10 older adults (mean age 73, range 67-79). Dilated pupils ranged from 6 to 7mm across subjects. Refraction was carried out with an automated refractor (Nicon 7001), using both objective and subjective techniques, which was then followed by acuity measurement using the same instrument. Table 2 lists these data, which strongly demonstrate that refractive error and acuity were not si~ifi~nt~y affected by dilation in either age group. These findings imply that optical blur is not a confounding variable in the contrast sensitivity data reported in Expt 2. Results The results of this experiment are best described by referring to Figs 4 and 5. Figure 4 displays the results for young subjects; Fig, 5, older subjects. Within each figure, Panel a contains data from 107 cd/m’; Panel b, 3.38 cd/ m*; Panel c, 0.107 cd/m2. Contrast sensitivity is plotted as a function of spatial frequency on log-log coordinates. In each graph, the dashed line with filled symbols represents performance with natural pupils (from Expt 1). The other functions on each graph represent how subjects performed when viewing with pupils of various sizes, as labelled on the graphs. In Fig. 5, which contains the data from the older group, the natural pupil data from the young adults is also
1242
MICIUEL E. SLOANEet
af.
Table 2. Refractive error and acuity with natural and dilated pupils Natural YoungM SEM Old M SEM
-0.28 0.16 +2.01 0.27
Refractive error’ Dilated Mean change’ +0.10 0.15 +2.11 0.31
0.38 0.09 0.11 0.09
Acuity2 Dilated Mean change4
Natural 0.91 0.04 1.24 0.06
0.83 0.02 1.28 0.08
-0.08 0.05 -0.02 0.05
‘Spherical equivalents. ZMin arc. )Mean difference in refractive error (Dilated-Natural) across subjects. 4Mean difference in acuity (Dilated-Natural) across subjects.
plotted by the dash-dotted line for comparison purposes. In both Figs 4 and 5, the natural pupil function is typically the highest function on each graph, indicating that subjects were most sensitive at each luminance level when viewing with their natural pupil. This effect is rather slight, yet worth noting because of its consistency
across panels. This was not only true for the group data as depicted in Figs 4 and 5, but also the case for most of the individual subjects (for 100% of older adults and 63% of young adults in at least two of the luminance conditions). Two additional observations can be made. First, providing older adults with larger pupils clearly did not improve their contrast sensitivity, even when their pupil sizes were increased to the
Old 107cd/m2
2.5
*Nat’1
1.0 0.5
0 > 6.5 A 6-6.5 0 5.25O(5mm
-
pupil 3.8mm mm mm 5.75mm
I
I
0.5 3.38
2.5
0 5.25-5.75mm OX
t
Young
F
1.5
3
0.5
5mm
cd/m2 Old 3.38
f e E::
(01
(b)
cd/m*
1.0 l
Nat’1
pupil
4.8mm I
I
*Not’1
3
_I Young
0.107
2.5 2.0
t
fwt’l
pupil
4.2mm
*
t
(cl
cd/m2
l
0.5
pupil 5.8mm
l
Spatial frequency
Wdeg)
Fig. 4. Mean contrast sensitivity for young adults as a function of spatial frequency. Subjects viewed with pupils of various sizes. Panel a, 107 cd/m2; Panel b, 3.38 cd/m2; Panel c, 0.107 cd/m2. Dashed line with solid circles is data with natural pupil. Functions with open symbols ___ and solid _ lines are data with dilated pupils (as indicated m ftgure).
B
Nar’i
pupil 4.2
mm
1 Spatial
frequency
(c/dag)
Fig. 5. As in Fig. 4, except for older adults. I)ash-dotted line (without symbols) is data from young adults with natural rxmits, included for com~~son purposes. _ .
Aging, senile miosis and spatial. vision
approximate size of the younger adult’s natural pupil. Second, for both young and older adults, pupil diameter did not have a substantial effect on spatial contrast sensitivity at any luminance level, which is in good agreement with a recent study on younger adults (Kay and Morrison, 1987).
GENERAL DISCUSSION
This study has indicated that older adults, even when considered clinically normal, tend to experience significant losses in spatial contrast sensitivity which are exacerbated under low environmental light levels. Older adults in this study exhibited contrast ~nsiti~ty reductions at all light levels tested, but their vision loss was especially significant at the lowest luminance. For example, at 0.107 cd/m2 older adults required approximately three times more contrast to detect a grating of intermediate spatial frequency than did young adults. The results from Expt 2 strongly suggest that senile miosis is not responsible for older adults’ contrast sensitivity deficits at any luminance tested. When older adults’ pupils matched the pupil size that naturally occurs in young adults at that light level, older observers still exhibited approximately the same magnitude of vision loss. In addition, these data imply that older adults’ contrast sensitivity loss at any of the tested light levels cannot be compensated for by a simple increase in diameter of the entrance pupil. Interestingly, older adults’ best contrast sensitivity was often with their own natural pupil, despite the fact that it was miotic at the lower light levels and thereby reduced retinal illumination. Contrary to common claims in the literature, it is incorrect to suggest that senile miosis is a detriment to older adults’ spatial vision; rather, senile miosis does not appear to hamper contrast sensitivity, and in some cases, is a “hidden” asset in that it slightly improves their spatial contrast sensitivity. Why might this be? One possibility may be related to the fact that the older eye has increased optical density of the ocular media, particularly the crystalline lens (Weale, 1963), which increases intraocular light scatter thereby degrading the retinal image and reducing image contrast. A smaller pupil may actually be an asset under these cimumstances, since it limits optical aberration and improves depth-of-focus, which facilitates image formation in the older eye.
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Our data also indicate that contrast sensitivity in younger adults was largely unaffected by changes in pupil, except for the tendency for the natural pupil to provide slightly better contrast sensitivity, as was the case in older adults. This slight natuml-pupil advantage is reminescent of Woodhouse’s finding (1975) that the natural pupil in younger adults tends to optimize spatial resolution under a variety of luminance conditions. In addition, our data are in good agreement with Kay and Morrison (1987) who report that contrast sensitivity (up to 30 c/deg) in younger adults was remarkably similar despite variations in pupil diameter. In a classic study on spatial vision, Campbell and Green (1965) also examined the role of pupil size in contrast sensitivity, but they were interested in the role of pupil size per se, in that they compensated for changes in pupil diameter with changes in illumination in order to keep retinal illuminance constant. They found that under these circumstances, pupil size did have a significant effect in that smaller pupils improved high spatial frequency sensitivity, since optical aberration was minimized. However, in the present study, our interest was in pupil size in a natural environment where ambient luminance level is not artificially altered to counteract changes in pupil diameter. Since senile miosis does not appear to be a causative factor in older adults’ loss in spatial contrast sensitivity, what other factors may be responsible? For a number of reasons, the crystalline lens is likely to have some role, although the extent of its contribution is unclear. Recent research has indicated that the modulation transfer function (MTF) of the excised, aged lens is markedly diminished at intermediate and high spatial frequencies, as compared to the MTF of the young adult lens (Block and Rosenblum, 1987). The older lens apparently attenuates the imaged contrast of higher spatial frequencies to a greater degree than does the young lens, implying that older adults would require more contrast to detect a higher frequency target than would young adults, which agrees with the psychophysical data (Derefeldt et al., 1979; Owsley et al., 1983). Block and Rosenblum (1987) argue that the MTF changes in the lens are most likely due to increased intraocular light scatter by the aged lens. While this MTF change in older adults could theoretically increase their contrast threshold at a given light level, it cannot account for the fact that older adults’ loss in spatial vision grows worse with
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MICHAELE.
decreasing luminance, since the MTF of the lens is invariant across mean light level, Thus it seems that we must look for additional factors underlying older adults’ loss in spatial vision. Other researchers have investigated the role of intraocular light scatter in older adults’ contrast threshold elevations. Allen and Vos (1967) measured the amount of backscattered light emerging from the eye in individuals ranging in age from childhood to the 80’s and also measured their contrast thresholds for Landolt-ring targets. They found that there was little relationship between the two variables; individuals with high levels of scatter did not have higher thresholds. 3ut one problem with their methodology is that the optical characteristics of backscattered light do not bear a close resemblance to forward scattered light, which is relevant in retinal image formation (see Paulsson and Sjostrand, 1980). More recently, Hemenger (1984) has argued that increases in intraocular scatter in the aged eye can account for increases in their contrast thresholds. In a mathematical argument based on disability glare data from Walraven (1973) and Vos (1965), Hemenger suggests that older adults’ contrast sensitivities loss can be attributed to intraocular light scatter since the ratio of the MTFs of the ocular media in the older vs younger eye is in good agreement with the ratio between their contrast sensitivity. But this conclusion may be somewhat questionable. First, some of the data points from Derefeldt et al. (1979) plotted in Hemenger’s Fig. 1 (1984; p. 1973) appear to be m&plotted; in addition, the data from Owsley et al. (19831, referred to in the Hemenger paper, are not included on the graph. A new graph has been generated including these additions and corrections and is displayed in Fig. 6. It is not clear that a light-scatter explanation closely fits the pattern of the contrast sensitivity data. The light scatter functions at first drop quite rapidly as a function of spatial frequency, and then level off around lOc/deg, whereas the contrast sensitivity data at first drop rather gradually, and then more rapidly with increasing spatial frequency. While light scatter may contribute to elevating contrast thresholds, there certainly appear to be other factors involved. It is also unclear how increased intraocular light scatter could account for older adults’ increased impairment in sensitivity at low light levels. Another lens-related factor that could interfere with contrast sensitivity is the lens’s increased light absorption with advancing age
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Fig. 6. Eased on Hemenger’s Fig. 1 (1984, p. 1973). The three curves, digitized from Hemenger’s graph and replotted, represent the ratio between the MTF of the older eye (age 65) and the MTF of the young eye (age 30), where a term for intraocular light scatter is explicitly included in the calculation of the MTF, based on Walraven’s (1973) measurements on the angular dependence of disability glare as a function of age (see Hemenger for further details). Each function represents a different width of the light scatter function, as labelled. Open triangles are based on Derefeldt et af.‘s (1979) contrast sensitivity data, plotted as the ratio of older adults’ sensitivity (age 60-70) to younger adults’ sensitivity (age 2t3-40). Open circles are the analogous data from Owsley et al. (1983).
(Said and Weale, 1959), which reduces retinal illuminance. This decreased retinal illuminance would lower the adaptation level of the retina and thus decrease contrast sensitivity, particularly at higher spatial frequencies (Kelly, 1972), as discussed earlier. If increased lens absorption was solely responsible for older adults’ contrast sensitivity loss, one would expect that the slope of the function relating contrast sensitivity and luminance would be equal for younger and older adults, with the older adults’ function simply displaced downward on the sensitivity axis. A recent study in our laboratory has indicated that older adults’ function does have a steeper slope (Sloane et al., 1988) suggesting that an explanation based solely on light absorption differences in the young vs old eye is inadequate in explaining older adults’ contrast sensitivity deficit. In conclusion, this study has indicated that senile miosis is not responsible for older adults’ loss in spatial contrast sensitivity. From the above discussion though, it is likely that increased intraocular light scatter and increased light absorption in the aged eye contribute to older adults’ contrast sensitivity deficit; further research must be designed to specifically quantify the magnitude of their involvement. However, these optical factors alone are inadequate for fully explaining why older adults’ loss in spatial contrast sensitivity becomes exacerbated
Aging, senile mia sis and spatial vision
with decreasing light level. Future studies must include parallel investigations into the role of neural mechanisms in older adults’ loss in spatial vision. Ac~ow~e~ge~ents-his research was supported by NIH grants AGO4212, EYO6390, and EYO3039 (Core) and a grant from Research to prevent Blindness Inc. to the UAB Department of Ophthalmology. We thank Bill Rosenblum, Michael Block, and Larry Mays for helpful discussion and Toby Basan for assistance during data collection,
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